Molecular Ecology (2011)
doi: 10.1111/j.1365-294X.2011.05240.x
Society, demography and genetic structure in the spotted
hyena
K A Y E . H O L E K A M P , * † J E N N I F E R E . S M I T H , * †‡ C H R I S T O P H E R C . S T R E L I O F F , †§ – R U S S E L L C .
V A N H O R N * * and H E A T H E R E . W A T T S * ††
*Department of Zoology, Michigan State University, 203 Natural Sciences, East Lansing, MI, USA, 48824-1115, †BEACON Center
for the Study of Evolution in Action, 1441 Biomedical and Physical Sciences Building, Michigan State University, East Lansing, MI,
USA, 48824, ‡Department of Ecology & Evolutionary Biology and Center for Society & Genetics, University of California Los
Angeles, 621 Charles E. Young Drive South, Los Angeles, CA 90095-1606, §Department of Microbiology & Molecular Genetics,
Michigan State University, 6130 Biomedical Physical Science Building, East Lansing, MI, 48824-4320, –Department of Ecology &
Evolutionary Biology, University of California Los Angeles, Terasaki Life Sciences Building, 610 Charles E. Young Drive East, Los
Angeles, CA 90095-7239, **Institute for Conservation Research, San Diego Zoo Global, 15600 San Pasqual Valley Road, Escondido,
CA 92027-7000, ††Department of Biology, Loyola Marymount University, 1 LMU Drive, MS 8220, Los Angeles, CA 90045, USA
Abstract
Spotted hyenas (Crocuta crocuta) are large mammalian carnivores, but their societies,
called ‘clans’, resemble those of such cercopithecine primates as baboons and macaques
with respect to their size, hierarchical structure, and frequency of social interaction
among both kin and unrelated group-mates. However, in contrast to cercopithecine
primates, spotted hyenas regularly hunt antelope and compete with group-mates for
access to kills, which are extremely rich food sources, but also rare and ephemeral. This
unique occurrence of baboon-like sociality among top-level predators has favoured the
evolution of many unusual traits in this species. We briefly review the relevant socioecology of spotted hyenas, document great demographic variation but little variation in
social structure across the species’ range, and describe the long-term fitness consequences of rank-related variation in resource access among clan-mates. We then
summarize patterns of genetic relatedness within and between clans, including some
from a population that had recently gone through a population bottleneck, and consider
the roles of sexually dimorphic dispersal and female mate choice in the generation of
these patterns. Finally, we apply social network theory under varying regimes of resource
availability to analyse the effects of kinship on the stability of social relationships among
members of one large hyena clan in Kenya. Although social bonds among both kin and
non-kin are weakest when resource competition is most intense, hyenas sustain strong
social relationships with kin year-round, despite constraints imposed by resource
limitation. Our analyses suggest that selection might act on both individuals and
matrilineal kin groups within clans containing multiple matrilines.
Keywords: dispersal, dominance, genetic diversity, population bottleneck, kinship, sex ratio,
social network
Received 23 February 2011; revision received 6 June 2011; accepted 20 June- 2011
Introduction
Long-term, individual-based studies of free-living animals offer uniquely rich opportunities for documenting
Correspondence: Kay E. Holekamp, Fax: (517)432-2789;
E-mail: [email protected]
2011 Blackwell Publishing Ltd
the kinship structure of populations, assessing effects of
particular phenotypic traits on fitness, and identifying
causes of individual variation in reproductive success
(Altmann & Altmann 2003; Clutton-Brock & Sheldon
2010). Longitudinal field studies with known pedigrees
that span multiple generations have now provided countless insights into important ecological and
2 K. E. HOLEKAMP ET AL.
evolutionary processes in natural populations (e.g. Clutton-Brock 1988; Schwartz et al. 1998; Kruuk et al. 2000;
Altmann & Altmann 2003; Wroblewski et al. 2009). In
combination with recent advances in molecular techniques, these enduring research programs continue to
shed considerable new light on relationships among
sociality, demography and genetic structure in animal
populations across multiple ecological time scales.
Long-term field study of the spotted hyena (Crocuta
crocuta) offers particularly interesting opportunities for
elucidating relationships among sociality, demography
and genetic structure in an unusually gregarious mammalian carnivore. These large predators live in societies
that are far larger and more complex than those of any
other mammalian carnivore (Drea & Frank 2003; Holekamp et al. 2007). With respect to their size, composition
and structure, spotted hyena groups, called ‘clans’,
more closely resemble the social groups of cercopithecine primates than those of other carnivores. Specifically, the size, composition and organizational structure
of spotted hyena clans are remarkably like those of
troops of baboons, macaques or vervet monkeys (Holekamp et al. 2007). As in troops of these primates, priority
of access to resources in any particular hyena clan is
determined by an individual’s social rank. Furthermore,
as in a cercopithecine primate troop, a hyena clan may
contain several different matrilineal kin groups spanning multiple generations concurrently. Thus hyena
clans contain many unrelated individuals as well as
close kin, and it is with this genetically diverse group
of clan-mates that spotted hyenas must contend in both
competitive and cooperative interactions (Van Horn
et al. 2004a; Smith et al. 2010). Like savannah baboons
(Papio cynocephalus, e.g. Alberts 1999; Buchan et al.
2003), spotted hyenas can discriminate both maternal
and paternal kin from unrelated clan-mates, and they
direct nepotistic behaviour toward both types of kin
(Kruuk 1972; Holekamp et al. 1997a; Van Horn et al.
2004b; Wahaj et al. 2004). However, in contrast to
baboons or other cercopithecine primates, spotted hyenas are top predators that regularly hunt antelope, and
compete with group-mates for access to ungulate carcasses when kills are made.
Fresh carcasses represent extremely rich food sources,
but they are also rare and ephemeral, occurring unpredictably in space and time. Therefore, competition at
kills is often very intense within clans (Frank 1986;
Holekamp et al. 1993), even among closely-related animals (Wahaj et al. 2004). On the other hand, spotted
hyenas routinely form coalitions with their kin to
defend carcasses from unrelated conspecifics (e.g. Engh
et al. 2005; Smith et al. 2010), and they also routinely
join forces with unrelated clan-mates to advertise and
defend their group territories, and to defend their kills
against lions or hyenas from neighbouring clans (Boydston et al. 2001; Van Horn et al. 2004a; Smith et al.
2008). The unique occurrence of baboon-like sociality in
well-armed predators occupying the highest trophic
positions in African ecosystems has favoured the evolution of many unusual traits in this species, including
females that are highly ‘masculinized’ with respect to
both their morphology and their behaviour (e.g. Watts
et al. 2009). That is, adult females are larger and more
aggressive than adult males, they are socially dominant
to all adult males born elsewhere, and the female’s genitalia are heavily ‘masculinized’ (Kruuk 1972; Frank
1986; Hamilton et al. 1986; Mills 1990; Szykman et al.
2003; Van Meter 2009). These unusual traits not only
give females top priority of access to food, but they also
give females virtually complete control over mating
(East et al. 1993).
In light of the unusual traits expressed in this species,
our goal here is to examine the relationship between
social organization and genetic structure within and
among hyena social groups. We focus in particular on
the role of kinship in hyena societies, and assess how
this varies with demographic and ecological conditions.
We begin by synthesizing published findings from
short- and long-term field studies of spotted hyenas
across their geographic range to elucidate variation in
demography and sociality. We find that, although clan
size and population density vary enormously, clan
structure and social organization are remarkably constant throughout the species’ range. We then use data
from our own 23-year, individual-based study of spotted hyenas in Kenya to summarize the long-term fitness
consequences of rank-related variation in resource
access among female clan-mates. Here we find that high
social rank confers a large fitness advantage after only a
few generations, but also that some low-ranking matrilines persist despite their relatively poor access to
resources, suggesting that chance plays a role in determining long-term matrilineal representation in hyena
populations. Next, based on our own field work, we
review patterns of genetic relatedness within and
between clans, and consider the roles of sexually dimorphic dispersal and female mate choice in the generation
of these patterns.
Finally, we apply social network theory to examine
effects of both matriline membership and variation in
ecological conditions on social relationships among clan
members. In contrast to baboon troops, which are
highly cohesive, spotted hyena clans are fission–fusion
societies; these are stable social units in which individual group members are often found alone or in small
subgroups, and in which subgroup size and composition change frequently over time (Kruuk 1972; Mills
1990; Smith et al. 2008). Fission–fusion dynamics permit
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HYENA SOCIETY, DEMOGRAPHY AND GENETICS 3
spotted hyenas to adjust grouping patterns in response
to both short-term and seasonal fluctuations in local
prey abundance (Holekamp et al. 1997b; Höner et al.
2005; Smith et al. 2008, 2011). Indeed, feeding competition constrains social relationships in this species, and
spotted hyenas adjust their grouping patterns over both
short- and long-time scales in response to competition
intensity, spending more time with conspecifics during
periods of abundant prey, and joining clan-mates at
kills in numbers correlated with the energetic value of
prey (Holekamp et al. 1993; Smith et al. 2008). As is the
case in most primate species (reviewed by Widdig
2007), individual hyenas are known to associate more
closely with kin than with non-kin (Holekamp et al.
1997a; Van Horn et al. 2004b; Wahaj et al. 2004), but it
is unclear to what extent matrilineal kinship affects
social network structure in the face of varying prey
abundance; we address this question here for the first
time.
Methods
Study species
Throughout their geographic range, which covers most
of sub-Saharan Africa, spotted hyenas form clans whose
members all know one another individually, rear their
cubs together at a communal den, and who also usually
cooperatively advertise and defend a group territory.
The stable core of any spotted hyena clan is comprised
of one to several matrilineal kin groups (Fig. 1), each
containing multiple adult females and their young
(Frank 1986; Mills 1990). In addition, each clan also contains one to several adult immigrant males. Because the
lifespan of wild spotted hyenas may exceed 18 years
(Drea & Frank 2003), but the average age at first reproduction is only 3.5 years (Holekamp et al. 1996), individuals from up to five different generations may be
present concurrently within the clan. Thus, hyena clans
are comprised of a number of different matrilineal kin
groups, each containing multiple overlapping generations of long-lived individuals. These group characteristics, in combination with rank-related resource access
and cognitive abilities allowing hyenas to remember
past social interactions, give rise to a social structure far
more complex than that found in any other mammalian
carnivore (Holekamp et al. 2007).
Like baboon troops, hyena clans are rigidly structured
by hierarchical rank relationships that determine priority of access to food (Tilson & Hamilton 1984; Frank
1986; Henschel & Skinner 1987; Smith et al. 2011).
Among all clan members except young cubs who have
not yet learned their status, rank relationships are usually unambiguous, such that there is a clear dominant
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Dominance rank order
Matriline 1
Matriline 2
Matriline 3
Matriline 4
Matriline 5
1.
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
14.
15.
16.
17.
18.
19.
20.
21.
22.
23.
24.
25.
26.
27.
28.
29.
BSH
MRPH
SEIN
GIL
BB
KIP
WHO
MALI
HG
JJ
MP
GER
NAV
SX
UA
BAIL
HOB
GOL
LG
MIG
NICK
POS
EXC
ZIP
DAY
BOS
EXV
RAR
JUBA
Philopatric
adult
females
Immigrant
adult
males
Fig. 1 Dominance rank order of matrilines within one cohort
of adults present in a single large clan. The dominance hierarchy of natal animals contains multiple matrilineal kin groups,
shown at left; each matriline is represented by a different shade.
Squares in genealogies represent males and circles represent
females. Although only adult females are shown among the
natal animals in the vertical listing at right, offspring are
included in the genealogies shown at left; offspring slot into
the hierarchy immediately below their mothers. Thus all adult
females and their young outrank all immigrant males.
and a clear subordinate within every dyad (Engh et al.
2000). Members of a particular matriline usually occupy
adjacent rank positions within the clan’s dominance
hierarchy (Fig. 1). Hyenas of both sexes maintain their
maternal ranks as long as they remain in the natal clan;
this means females retain their maternal ranks throughout their lives, but males retain them only until they
emigrate (Smale et al. 1993, 1997).
Whereas female spotted hyenas are strongly philopatric, nearly all males emigrate from their natal clans after
they become reproductively mature; natal dispersal
usually occurs between 2 and 5 years of age (Smale
et al. 1997; Boydston et al. 2005; Höner et al. 2007).
Many prospective immigrant males visit neighbouring
groups each year on brief ‘prospecting’ forays, but only
a small fraction of these males ever become socially
integrated such that they assume positions in new clans
as long-term resident males. In addition to resident
immigrant males, so called when they are continuously
present for at least 6 months, each clan may also contain one or more adult natal males (e.g. those older than
24 months) that have not yet emigrated (Henschel &
Skinner 1987; Holekamp & Smale 1998; Höner et al.
2005). In habitats where dispersal opportunities are limited, some males may even spend their entire lives in
their natal clans (e.g. Höner et al. 2007).
All natal hyenas are socially dominant to all immigrants (Kruuk 1972; Frank 1986; Mills 1990; Smale et al.
4 K. E. HOLEKAMP ET AL.
1993). Thus adult females and their offspring can displace adult immigrant males from food; this benefit of
rank accrues even to very young cubs. In fact, in 30min focal animal surveys during which juveniles were
feeding on kills when adult immigrant males were also
present, only once out of 572 surveys did a juvenile
allow an immigrant to feed (Van Horn et al. 2004b).
The mechanisms by which social rank is acquired differ
between immigrant males and natal hyenas. Regardless
of their maternal rank in the natal clan, when males
emigrate they appease all new hyenas they encounter,
so they enter a new clan at the very bottom of its overall dominance hierarchy (Smale et al. 1997). Thus, priority of resource access inevitably declines dramatically
after dispersal for sons of high- and low-ranking
females alike. Nevertheless, virtually all males emigrate
from their natal clans voluntarily; they are not driven
out by conspecifics, nor do their ranks fall before dispersal (Smale et al. 1997). Ranks of immigrants within
the male hierarchy are determined by arrival order in
the new clan, because males conform to a strict queuing
convention (Smale et al. 1997; East & Hofer 2001). By
contrast, natal hyenas assume positions in the clan’s
dominance hierarchy immediately below those of their
mothers. This occurs during a long, intensive period of
social learning early in postnatal development (Holekamp & Smale 1991, 1993; Smale et al. 1993; Engh et al.
2000).
Although rank relationships among adult clan-mates
are generally very stable over long periods of time,
changes in rank relationships do sometimes occur, indicating that rank is not genetically determined in this
species. For example, an animal’s rank can fall substantially within its lifetime due to recruitment of daughters
of higher-ranking females, and rank reversals may
occur within matrilines, particularly when adult daughters overtake their aging mothers. Furthermore, entire
matrilines occasionally reverse their rank order after
major fights. That is, revolutionary coalitions sometimes
form among members of a low-born matriline to overthrow a smaller but higher-ranking matriline (e.g. Mills
1990; Hofer & East 1996). Collectively these facts suggest that social rank is too labile to be directly determined by behavioural or morphological traits that are
strongly heritable; in fact, results from several studies
indicate absence of direct genetic influences on offspring rank (Mills 1990; Holekamp et al. 1993; Engh
et al. 2000; East et al. 2009).
Spotted hyenas breed year-round throughout their
range, although some populations have birth peaks or
troughs that are temporally associated with varying
prey abundance (Holekamp et al. 1999). The mating
system of the spotted hyena is polygynandrous. Both
males and females mate promiscuously, and no endur-
ing pair bond develops between the sexes (Szykman
et al. 2001; Engh et al. 2002; East et al. 2003). Females
have been observed to mate with up to three males during a single estrous period, and members of both sexes
have been known to copulate with several different
mates over the course of several years (Engh et al.
2002). Many twin litters are sired by multiple males
(Engh et al. 2002; East et al. 2003). Females usually bear
litters of one or two cubs in dens, where cubs are sheltered for the first 9–14 months of their lives. Weaning
occurs very late in spotted and other bone-cracking hyenas compared to all other mammalian carnivores of the
same or larger body size (Watts et al. 2009); hyena cubs
are typically weaned when they are 12–18 months old
(Holekamp et al. 1996). Spotted hyenas of both sexes
are physiologically competent to breed by 24 months of
age (Glickman et al. 1992; Dloniak et al. 2006), although
most individuals delay reproduction for at least another
year after puberty (Holekamp et al. 1996).
Methods used in our review of the literature
We reviewed patterns of demography and social organization described in 23 published studies of spotted
hyenas, and extracted data documenting population
density, clan size, home range size, sex ratio among
adult clan members, and percent of each clan comprised of adults. We report home range size in square
kilometres, and in most cases home range size is synonymous with the size of the average territory defended
by clans in a particular part of Africa. However, in
some regions, spotted hyenas do not engage in active
territorial defence or boundary marking, and in those
cases, home range size is determined based strictly on
patterns of space use by clan members. Where spotted
hyenas defend territories but also travel well outside
the boundaries of their territories to forage, we report
mean size of defended territories as home range size.
Values for hyena density and mean clan size are as
reported in the original field studies.
Observational methods in our long-term field study in
Kenya
We focus here most heavily on insights gleaned from
our long-term study of one large social group in the
Talek region of the Masai Mara National Reserve,
Kenya (henceforth, the Mara). We have observed the
Talek clan continuously since June 1988, and L. G.
Frank (1983, 1986) monitored it before us, from 1979 to
1987. We also assess the generalizability of our findings
among clans. We currently work with six Mara clans,
and from 2003 to 2005, we also monitored two large
clans in Amboseli National Park. We employ the same
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HYENA SOCIETY, DEMOGRAPHY AND GENETICS 5
observational methods in each clan. That is, we recognize all individual hyenas by their unique spot patterns,
and sex them based on the dimorphic morphology of
the erect phallus (Frank et al. 1990). Assignment of an
individual’s social rank within its clan is based on its
position in a matrix ordered by submissive behaviour
displayed during dyadic agonistic encounters (Martin &
Bateson 1986; Engh et al. 2002; Smith et al. 2011). Using
field vehicles as mobile blinds, researchers observe hyenas 21–31 days each month, recording which individuals are present, and all occurrences of agonistic
interactions. We initiate an observation session each
time we encounter one or more hyenas separated from
other clan members by at least 200 m; hyenas in different sessions are typically separated by at least 1 km
(Smith et al. 2008). Upon arrival at each session, and
during subsequent scans performed every 15–20 min,
we record the identity and activity of every hyena in
that focal subgroup. Sessions last from 5 min to several
hours, and end when we leave an individual or group.
We use these session data below as we apply social network theory to assess the effects of kinship on social
relationships among members of the Talek clan as they
cope with varying ecological conditions.
Genotyping and assessment of relatedness within and
among clans and populations
To evaluate patterns of relatedness within and among
clans of spotted hyenas in the Mara and Amboseli, individual hyenas from both populations were genotyped
at 8–12 microsatellite loci using DNA extracted from
blood, tissue or faeces (Van Horn et al. 2004a; Watts
et al. 2011). Pairwise relatedness values (R) based on
both maternal and paternal kinship were estimated for
individuals sampled from each population using the
program RELATEDNESS 5.0 (Queller & Goodnight
1989). All microsatellite loci were in Hardy–Weinberg
equilibrium in both Mara and Amboseli populations.
Patterns of R were examined using longitudinal data
collected on the Talek clan and cross-sectional data collected on multiple clans in both populations (Mara,
N = 335 genotyped hyenas; Amboseli, N = 80 genotyped hyenas). Population comparisons were based on
samples from two clans of hyenas in each park, collected during overlapping 2-year periods. Clans were
similar in size in both populations, and covered similar
geographic sampling areas (Watts & Holekamp 2008).
Finally, to assess the scope of kin-biased dyadic interactions in the clan, we used data from Smith et al. (2010)
to calculate the number of dyadic pairs present in the
clan for a large cohort (N = 31) of adult females present
concurrently in the Talek clan from January, 1996 to
December, 2000. This was a period of social stability
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occurring between clan fission events. We assigned 222
pairs of adult females present during this period to one
of the three following kinship categories based on their
maternal and paternal relationships: close kin (coefficient of relatedness (r) = 0.5; mother–daughter or full
sisters), distant kin (r = 0.125–0.25; grandmother–granddaughter, maternal or paternal half sisters, aunt–niece)
or non-kin (r 0.00).
Assessment of reproductive skew
To quantify the degree of reproductive skew among
Talek hyenas, we calculated Nonacs binomial skew
index B (Nonacs 2000, 2003), using the software SKEW
(Nonacs 2003; http://www.eeb.ucla.edu/Faculty/Nonacs/shareware.htm). Nonacs’ skew index B ranges
from )1 to +2; positive values indicate that skew is
greater than expected, and negative values indicate that
skew is less than expected such that reproduction is
more evenly distributed than expected. B = 0 indicates
random mating. Because the accrual of a reproductive
benefit (i.e. a cub) could only be assessed for males via
genetic paternity analysis (Engh et al. 2002; Van Horn
et al. 2004a), this constrained the set of potential benefits, and the set of potential beneficiaries, to hyenas that
were genotyped. Because variation in survival, or tenure in a group, can produce reproductive skew aside
from an impact of any behavioural interactions (Crespi
& Yanega 1995), we calculated tenure within the clan
for each potential beneficiary (i.e. immigrant male, or
adult natal male or female) within the dates set by the
conceptions of the cubs for which paternity was known.
We estimated the one-tailed P value associated with the
observed B for females, and for males, relative to the
random accrual of reproductive benefits, via 10 000 simulations. We also used 10 000 simulations in our power
analysis, and we generated the two-tailed 95% C.I. for
B.
Methods used to analyse the effects of kinship and prey
abundance on social network structure
To evaluate the persistence of maternal kinship effects
in structuring social networks within the Talek clan in
the face of fluctuating food availability, we documented
variation in local prey abundance at biweekly intervals
throughout our longitudinal study, as described by
Cooper et al. (1999). Although paternal kinship may
further structure social relationships within clans, we
were specifically interested in elucidating the persistence of long-term social network structure, and knowledge of paternity was unavailable for the early years of
our long-term study. Therefore, here we considered
natal dyads belonging to the same matriline within the
6 K. E. HOLEKAMP ET AL.
Talek clan (e.g. grandmother–grandchildren, mother–
offspring, maternal sister and half-sister pairs) to be
maternal kin, and natal hyenas from different matrilines
to be non-kin. These relationships were established
based on pedigree construction using genetic parentage
assignment (Engh et al. 2002; Van Horn et al. 2004a)
and nursing associations between mothers and offspring (Holekamp et al. 1993).
We assessed association patterns based on the cooccurrence of dyad members in observation sessions, as
done previously for this species (e.g. Holekamp et al.
1997b; Szykman et al. 2001; Smith et al. 2007). Briefly,
we calculated the Twice-Weight Association Index (AI)
of Cairns & Schwager (1987) for each pair of individuals, hyenas A and B, during the period for which they
were concurrently present in the clan. We calculated
AIA,B as: (A+Btogether) ⁄ [(Awithout B) + (Bwithout A) +
(A+Btogether)] where (A+Btogether) is the number of sessions in which A and B are present together, (Awithout B)
is the number of sessions in which A was present without B, and (Bwithout A) is the number of sessions in
which B was present without A.
We constructed a social network for each consecutive
4-month interval from 1988 through 2003. These intervals correspond to predictable seasonal variations in
prey abundance observed throughout our study (Holekamp et al. 1997b, 1999; Smith et al. 2008): one 4-month
period of superabundant prey (June to September) each
year, and two periods of relatively low prey density
(October to January and February to May). We assigned
a life history stage (cub, subadult or adult) to each
hyena using detailed demographic and genealogical
records, and estimated (to ±7 days) the ages of cubs
born in the clan when they were first observed above
ground, based on pelage, size, and behaviour (Holekamp & Smale 1998). Hyenas were considered to be cubs
while they were residing at dens. We considered hyenas to be den-independent subadults when we found
them more than 200 m from the current communal den
on at least four consecutive occasions; this usually
occurred when youngsters were roughly 9 months old
(Boydston et al. 2005). Here we considered natal males
older than 24 months to be reproductively mature
adults (Glickman et al. 1992; Curren LJ, Weldele ML,
Holekamp KE 2011, unpublished electroejaculation
data.), and classified females as adults at 36 months of
age or at their first known date of conception, whichever occurred first. If a hyena changed life history
stages during a 4-month sampling period, then it was
assigned to the life history stage it occupied at the midpoint of the sampling period.
We depict the Talek clan as a social network comprised of ‘nodes’ representing individual actors connected by associations, called ‘ties’ (Wasserman & Faust
1994). Each node within the network represents a natal
hyena present in at least five observation sessions during a sampling period. For each hyena within each network, we calculated the ‘strength’ of its social ties with
group-mates as the sum of its association indices with
all clan-mates in each of three categories (all natal hyenas, maternal kin, and non-kin), and divided each sum
by the number of other potential actors (minus the focal
hyena) in each network class. Defined this way, ‘standardized strength’ measures the extent to which each
hyena associates with all potential actors in the network
(Barthelemy et al. 2005). Because even weak associations are potentially important for the maintenance of
clan structure, we constructed weighted, unfiltered networks based on all associations (Croft et al. 2008; James
et al. 2009).
All statistical analyses of social networks were conducted using individual hyenas as sampling units. We
limited our analysis to those natal hyenas observed to
be in a particular life history stage during periods of
both low and high prey when both kin and non-kin
were available to them as social partners. If a particular
focal hyena occupied the same life history stage within
multiple networks, then we constructed a single mean
value across networks for that hyena. We used nonparametric statistics to analyze network traits because
we were unable to transform these non-normally distributed data, and we corrected for multiple testing
using sequential Bonferroni adjustments (Rice 1989).
Specifically, using STATISTICA 6.1, we compared means
between two, or among more than two, independent
groups using Mann–Whitney U and Kruskal–Wallis
tests, respectively. We compared the means of two
dependent groups using Wilcoxon-signed rank tests.
Differences between groups were considered significant
at alpha £0.05.
Results and Discussion
Variation in the demography and social structure of
spotted hyenas across their range
Spotted hyenas occupy an extraordinarily diverse array
of habitats in sub-Saharan Africa, including savanna,
deserts, swamps, woodland and montane forest. Densities of spotted hyenas vary by orders of magnitude
among these habitats. In the deserts of southern Africa,
hyena densities can be as low as one hyena per hundred square kilometres (Tilson & Henschel 1986; Mills
1990). The highest population densities reported for this
species occur on the prey-rich savannah plains of Kenya
and Tanzania (e.g. Kruuk 1972; Frank 1986; Höner et al.
2005; Watts & Holekamp 2008; Watts & Holekamp
2009), and surprisingly, in the montane forest of Aber 2011 Blackwell Publishing Ltd
HYENA SOCIETY, DEMOGRAPHY AND GENETICS 7
dare National Park in Kenya (Sillero-Zubiri & Gottelli
1992); in these areas, densities of spotted hyenas often
exceed one animal per square kilometer. However,
across 23 study populations the mean density was
0.45 hyenas ⁄ km2, ranging from 0.009 to 1.65
hyenas ⁄ km2 (Holekamp & Dloniak 2010).
In association with varying population densities,
clans range in size from the tiny groups found in the
Kalahari and Namib deserts, which may contain as few
as four or five members (Tilson & Henschel 1986; Gasaway et al. 1989; Mills 1990), to the large clans in eastern Africa, which may contain over 90 members (Kruuk
1972; Frank 1986; Hofer & East 1993a; Holekamp et al.
1993). Across 19 study populations in which all individual members were known for one or more clans, mean
clan size was 28.8 hyenas, but this ranged from 3 to 67
hyenas (Holekamp & Dloniak 2010), with the largest
clans occurring in the populations of highest density
(linear regression: r2 = 0.717, P < 0.0001, Fig. 2A).
The home ranges occupied by clans of spotted hyenas
also vary enormously with population density (Fig. 2B).
90
y = 29.435x + 13.599
R2= 0.5621, P = 0.0001
(A)
80
Mean clan size
70
60
50
40
30
20
10
0
0.0
0.2
0.4
0.6
0.8
1.0
1.2
1.4
1.6
1.8
2
Population density (hyenas/km )
1200
(B)
Table 1 Sex ratios among adult clan members, and percentage
of clan membership comprised of adults, in those populations
for which these data are available
log y = 1.53 – 0.606*log x
R2= 0.717, P < 0.0001
% clan
membership
comprised
of adults
800
Study area
Adult sex
ratio (# of
females ⁄
# of males)
600
Serengeti
Ngorongoro
Kalahari
Chobe
Kruger
1.2
1.2
2.5
3.1
2.5
63
69
36
56
73
Amboseli
1.7
46
Aberdares
1.0
—
Mara
Mara
x
1.8
1.5
1.8
47
48
55
1000
Home range (km2)
Home range size for clans studied throughout sub-Saharan Africa ranges from 13 to 1 065 km2, with a mean
of 169 km2 (Holekamp & Dloniak 2010). As population
density and the number of hyenas per clan increase,
home range size decreases, although this relationship is
non-linear (Fig. 2B: r2 = 0.562, P = 0.0001, following log
transformation of both variables). This pattern of
decreasing home range size with increasing population
density is similar to that found in other mammalian carnivores (e.g. Trewhella et al. 1988). This pattern is also
consistent with the hypothesis that habitat carrying
capacity for hyenas, as reflected in both clan size and
population density, is limited by food availability (Mills
1990). Indeed, in most parts of Africa, clan size
increases with local prey density (Trinkel et al. 2006).
However, in the Serengeti, large aggregations of migratory herbivores within commuting distance of hyena
territories permit a decoupling of clan size from prey
availability within the territory per se (Hofer & East
1993a; b). Furthermore, in the island-like habitat on the
floor of Ngorongoro Crater, mean size of seven resident
clans was more closely related to overall prey availability in the Crater than to that in the territory of any particular clan (Höner et al. 2005).
The small clans inhabiting the deserts of southern
Africa usually contain only one or two matrilines (e.g.
Mills 1990) and a single immigrant male, whereas the
large clans in the prey-rich plains of eastern Africa may
contain over 10 matrilines and several immigrant males
(e.g. Frank 1986). Among adult clan members, sex ratios
are at least slightly female-biased in most well-studied
populations (Table 1) and average 1.8 adult females for
every adult male. On average, clan membership is
400
200
0
0.0
0.2
0.4
0.6
0.8
1.0
1.2
1.4
1.6
1.8
Population density (hyenas/km2)
Fig. 2 Relationships between hyena density and (A) clan size
and (B) home range size for spotted hyena clans across subSaharan Africa. Data drawn from published studies listed by
Holekamp & Dloniak (2010) in their Table 3.
2011 Blackwell Publishing Ltd
Reference
(Hofer & East 1993a)
(Höner et al. 2005)
(Mills 1990)
(Cooper 1989)
(Henschel & Skinner
1987)
(Watts & Holekamp
2008)
(Sillero-Zubiri &
Gottelli 1992)
Current study
(Frank et al. 1995)
8 K. E. HOLEKAMP ET AL.
Fig. 3 Long-term variation in the composition of one large
clan in Kenya, the Talek clan. Here monthly mean composition
of the clan is averaged within year, from 1988 to 2010.
roughly evenly split between immature and mature
individuals (Table 1).
Of all the adult males present in a clan at a particular
time, adult natal males generally comprise 25–40%, and
the rest are immigrants (Holekamp & Smale 1998;
Höner et al. 2005, 2007). Figure 3 shows temporal variation over 22 years in the composition of one large clan
in Kenya. Relative representation in the clan of each
demographic sub-group remains surprisingly stable
over time. Clan size reached its apex in 2010, after
2 years of severe drought in Kenya, during which the
Talek hyenas had frequent access to dead cattle as well
as their normal prey base.
Effects of social rank on female fitness
The nature of the food resources on which spotted hyenas rely creates a competitive environment that shapes
hyena social relationships. Individual hyenas experience
strong direct and indirect selection to assist their kin in
attaining and maintaining social rank and the resources
to which their rank entitles them (Smith et al. 2010).
Because an adult’s social status determines its priority
of access to food during competitive interactions over
kills (Fig. 4), rank has profound effects on hyenas’
intake of calories and nutrients (Holekamp & Smale
2000; Hofer & East 2003). Furthermore, high social rank
also permits adult female spotted hyenas to reduce
energy expenditures demanded by long-distance travel
to remote feeding sites (Fig. 4). For example, subordinate females in Kenya are far less likely than dominant
females to forage in the central prey-rich areas of the
clan’s territory (Boydston et al. 2003). Where females
often hunt migratory antelope outside the boundaries
of the clan’s territory, as in the Serengeti, low-ranking
females need to commute to distant prey much more
Fig. 4 Schematic diagram showing how social rank mediates
reproductive success among adult female spotted hyenas. The
arrows running from left to right represent rank effects within
a generation. The bottom arrow indicates the positive feedback
of maternal kin joining forces on the maintenance of these rank
effects into the next generation. Footnotes indicate published
papers containing data that support claims in this diagram: (1)
Frank (1986) (2) Hofer & East (1993b); Holekamp et al. (1997b);
Boydston et al. (2003a); Kolowski et al. (2007); White (2006);
Höner et al. (2005); (3) Holekamp et al. (1996); Hofer & East
(1993c, 1996, 2003); Watts et al. (2009); Swanson et al. (2011);
(4) Holekamp et al. (1997a); Smith et al. (2008, 2010).
frequently than do high-ranking females (Hofer & East
1993a; b) The relatively high ratio of energy gain to
energy loss enjoyed by high-ranking female hyenas has
important consequences with respect to reproductive
success and life-history traits (Fig. 4).
All adult female clan-members breed, but initiation of
breeding efforts depends on immediate energy availability in this species, so females reproduce at rates that
increase with social rank (Frank et al. 1995; Holekamp
et al. 1996; Hofer & East 2003). High-ranking females
obtain more resources (Frank 1986; Holekamp & Smale
2000), and thus are able to provide better nourishment
to their cubs. The rank-related variation in females’ ability to access food has striking effects on the growth
rates of their cubs, with high-ranking cubs growing
much faster than their low-ranking peers (Hofer & East
1996, 2003). Dominant females can also wean their cubs
at much younger ages, and much smaller body sizes,
than can subordinate females (Frank et al. 1995; Holekamp et al. 1996; Watts et al. 2009).
The age at which females first bear young is strongly
correlated with maternal rank, with daughters of the
alpha female first giving birth at around 2.5 years of
age, and daughters of the lowest-ranking females doing
so at 5–6 years of age (Holekamp et al. 1996; Hofer &
East 2003). Although rank does not affect litter size in
hyenas, perhaps because females typically have only
two functional nipples, inter-litter intervals are much
shorter among dominant than subordinate females, and
2011 Blackwell Publishing Ltd
HYENA SOCIETY, DEMOGRAPHY AND GENETICS 9
dominants are more frequently able to support pregnancy and lactation concurrently. Therefore the annual
rate of cub production is substantially higher among
dominant than subordinate females (Holekamp et al.
1996). Maternal rank affects the likelihood that cubs will
survive to reproductive maturity, and it also has a pronounced effect on longevity among adult females;
daughters of high-ranking females live longer than do
daughters of low-ranking females (Watts et al. 2009).
Because both birthrates and survivorship are so much
greater among high- than low-ranking hyenas (Watts
et al. 2009), dominant hyenas tend to have many more
surviving kin in the population at any given time than
do subordinates (Figs. 1, 5), and thus they enjoy a
much larger network of potential allies, should the need
for those arise (e.g. Van Horn et al. 2004a; Smith et al.
2010). Because high-ranking females start breeding earlier, live longer, and produce more surviving cubs per
unit time, we have observed as much as a fivefold difference in lifetime reproductive success between the
highest- and lowest-ranking females in our Kenyan
study populations (Holekamp & Smale 2000). Thus a
female’s social rank has enormously important fitness
consequences. These effects, as they have accrued over
30 years, are shown in Fig. 5 for 19 adult females present in the Talek clan in 1979 (Frank 1983).
When L. G. Frank (1986) began working with the
Talek clan in 1979, he knew nothing about genealogical
relationships among adult females, but he was able to
discern their rank relationships based on outcomes of
Fig. 5 Rank-related variation in fitness among adult female
spotted hyenas. Cells in the 1979 column (from Frank 1983)
represent 19 adult females present in the Talek clan that year,
shown in descending rank order. Cells in the 1989, 1999, &
2009 columns represent descendants of those original 19
females, and their proportional representation in the clan. Gray
triangles represent extinction events for entire matrilines. Numbers of adult females present in the clan have ranged from 13
to 25 during this period.
2011 Blackwell Publishing Ltd
agonistic interactions, as described in ‘Methods’. In
Fig. 5, each of the 19 adult females present in the clan
in 1979 is assigned a different cell in the leftmost column, arranged in descending rank order, and cells in
subsequent columns represent this female and her
descendants, or her descendants alone. Of 19 adult
females originally present in the Talek study clan in
1979 (Frank 1983, 1986), only four had living descendants among the 22 adult females present in the clan in
2009 (Fig. 5). The alpha female in 1979, who then represented only 5% of the adult female population, gave
rise to over half the current adult females. Furthermore,
the descendants of the 1979 alpha and beta females
together now comprise nearly 80% of the adult female
population. Although it can be seen here that highranking females clearly enjoy a large fitness advantage
over subordinates, it is also clear from Fig. 5 that the
relatively low-ranking matriline deriving from female
F40 persists over many generations despite the energetic handicaps with which its members must cope.
This suggests that chance may play an important role
in determining which subordinate matrilines persist
over extended time periods.
Patterns of relatedness within and among hyena clans
and populations
The pattern apparent in Fig. 5 might lead the uninformed reader to expect that hyena clans should be relatively recently derived from a single high-ranking
ancestor, and that natal clan-mates might therefore be
expected to be closely related to one another. However,
our data show clearly that this is not the case. Estimated average R values for the Talek clan fit expectations among dyads of known genealogical relationships
(Fig. 6). Average genetic relatedness among natal members of the Talek clan was extremely low
(R = 0.011 ± 0.002, Van Horn et al. 2004a; Fig. 6), and
similar to R values for males immigrating into the Talek
clan from myriad neighbouring clans (mean R values
among adult immigrant males was 0.009 ± 0.007; Van
Horn et al. 2004a; Fig. 6). Nevertheless, Van Horn et al.
(2004a) found that average relatedness is greater within
than among matrilines of spotted hyenas, even across
successive generations, but also that relatedness is
diluted across generations within matrilines. Finally, the
decline in mean R values across territorial boundaries
separating neighboring hyena clans (Fig. 7) suggests
that most successful dispersal by male hyenas occurs to
nearby clans. This is consistent with dispersal distances
documented for radio-collared males born in our study
clans (Smale et al. 1997; Boydston et al. 2005).
Although the hyena populations in the Masai Mara
and Amboseli are currently quite similar with respect
10 K . E . H O L E K A M P E T A L .
0.5
Pairwise R-value
0.4
73
71
16
0.3
0.2
244
0.1
0
12 561
861
re
cu
b
Fu
lls
ib
H
al
fs
ib
N
at
al
Im
m
ig
ra
nt
Si
M
om
cu
b
–0.1
Pair type
Fig. 6 Pairwise R values within the Talek clan of any two
natal animals, any two resident immigrants and four types of
close kin: mothers and cubs (momcub), sires and cubs (sirecub), full-sibling pairs (fullsib) and half-sibling pairs (halfsib).
Sample sizes indicate number of R values. Mean values are
presented ±SE. Reproduced with permission from Van Horn
et al. (2004a).
Pairwise R-value
0.05
a
0
13 335
c
b
5494
d
9546
1760
–0.05
0
1
2
3
# of clan borders
Fig. 7 Pairwise R values for natal animals from the Talek clan
and six other clans are shown in relation to the number of clan
borders separating spotted hyenas; there are no clan borders
separating members of the same clan. Sample sizes indicate
number of R values. Mean values are presented ±SE. Reproduced with permission from Van Horn et al. (2004a).
to many demographic characteristics (e.g. Table 1),
their recent population histories differ markedly.
Whereas our Mara hyena study population has
remained consistently large since at least the late 1970s,
with a density of at least 0.86 hyenas ⁄ km2 (Frank 1986),
the population in Amboseli National Park experienced
a demographic bottleneck during the 1970s and 1980s,
in which a large population was reduced to approximately 50 individuals (C. Moss, personal communication; Faith & Behrensmeyer 2006), representing a
population density of only 0.13 hyenas ⁄ km2. The bottleneck appears to have lasted approximately 25 years;
based on an estimated generation time for spotted hyenas of 5.7 years (Watts et al. 2011), the bottleneck thus
spanned roughly four generations. In the mid-1990’s,
the Amboseli population exploded in size, likely resulting from changes in the local prey base and extirpation
of the local lion population by pastoralists, and reached
a population density of 1.65 hyenas ⁄ km2 by 2003–2005
(Watts & Holekamp 2008). Despite these historical differences between parks, patterns of relatedness among
natal animals were remarkably similar between Amboseli and the Mara (Watts et al. 2011). As in the Mara,
average relatedness was higher among Amboseli clanmates than among hyenas born and living in adjacent
clans. Moreover, we found no differences between the
populations in measures of genetic diversity (Watts
et al. 2011). Although the social and genetic make-up of
the ancestors of the current Amboseli population are
unknown, the relatively low levels of relatedness and
high levels of genetic diversity in Amboseli indicate it
is unlikely that they are descended from a group of closely related individuals.
The patterns of relatedness apparent in both our
Mara and Amboseli populations conform to the theoretical expectation (Lukas et al. 2005) that mean relatedness among natal clan members should be similar to
that among immigrants. These patterns in spotted hyenas are likely shaped by at least five factors. First, social
structuring by matrilines within clans, and by clans
within populations, most likely facilitates the maintenance of genetic diversity among natal hyenas (Sugg
et al. 1996). Second, clan sizes in both our Mara and
Amboseli study populations are quite large, and the
number of possible dyads per clan increases exponentially with the number of clan members (Lukas et al.
2005). High average relatedness among natal individuals is only expected in very small groups (Lukas et al.
2005). Third, mean R values are affected by the proportion of related dyads present in a clan at any give time,
and this is relatively small compared to the total number of dyads present. For example, when we used data
from Smith et al. (2010) to calculate and classify the
number of dyadic pairs present in the clan for a large
cohort (N = 31) of adult females, we found 222 adult
female dyads present concurrently in the Talek clan
from 1996 through 2000. Of these, only 11% (N = 25
dyads) were close kin (R = 0.462 ± 0.028), and 16%
(N = 36 dyads) were distant kin (R = 0.279 ± 0.040);
thus nearly three quarters of the 222 female dyads
2011 Blackwell Publishing Ltd
H Y E N A S O C I E T Y , D E M O G R A P H Y A N D G E N E T I C S 11
(73%, N = 161 dyads) were non-kin (R = )0.228 ±
0.006). Fourth, in both Mara and Amboseli populations,
patterns of relatedness are undoubtedly affected by
male dispersal behaviour. Specifically, immigration into
each clan of males from multiple neighbouring clans
contributes to low average relatedness within clans, as
well as to the maintenance of genetic variation. Furthermore, male spotted hyenas emigrate at high rates (East
& Hofer 2001; Boydston et al. 2005), causing a regular
influx of paternal genes via dispersing males. Male
spotted hyenas also exhibit great behavioural plasticity
(Mills & Hofer 1998; Boydston et al. 2003b; Hayward
2006; Kolowski & Holekamp 2009), which probably
facilitates their dispersal across potential barriers,
including areas with substantial anthropogenic activity.
Consequently, it is highly likely that there was migration into the Amboseli population from surrounding
areas, and just a few migrants into a small population
can be sufficient to maintain or restore genetic variation
(Keller et al. 2001; Vilà et al. 2003; Hogg et al. 2006).
Finally, the low mean relatedness among natal animals
in our study populations is likely caused in part by relatively low reproductive skew among resident male
hyenas (Engh et al. 2002; Holekamp & Engh 2009). We
discuss effects of dispersal and skew patterns further
below.
Effects of dispersal, mate choice and reproductive skew
on patterns of relatedness
Although male spotted hyenas are highly mobile, and
physically capable of traveling long distances quite
quickly (e.g. Hofer & East 1993a), their ability to join
new clans is evidently constrained by the severe aggression directed at potential immigrants by resident immigrant males (Smale et al. 1997; Boydston et al. 2001;
Szykman et al. 2003). Most habitats in which spotted
hyenas occur appear to be saturated such that clan territories form a mosaic covering the entire landscape (Kruuk 1972; Boydston et al. 2001). Each territorial border is
thus a potential barrier to dispersal. Most males successfully engaging in natal dispersal immigrate into clans
separated from their natal ranges by only one or two
territorial borders (Smale et al. 1997; Boydston et al.
2005; Höner et al. 2010). In contrast to lions and other
carnivores in which coalitions of related males often disperse together (e.g. Pusey & Packer 1987; Caro 1994),
male spotted hyenas disperse alone, such that resident
immigrant males represent a true mélange of clans, and
accordingly, relatedness among immigrants is extremely
low (Van Horn et al. 2004a; also see Fig. 6).
Although the mating system of the spotted hyena is
polygynous, matings are not monopolized by highranking males, and aggressive contest competition
2011 Blackwell Publishing Ltd
appears to have little influence on male reproductive
success (Engh et al. 2002; East et al. 2003). This is in
marked contrast to the situation in most other gregarious mammals (e.g. Hoelzel et al. 1999; Di Fiore 2003;
Alberts et al. 2006), where reproductive success is
strongly correlated with fighting ability and intra-sexual
rank. Instead, the strongest determinants of reproductive success among male spotted hyenas are dispersal
status, length of residence as immigrants in new clans
after dispersal, the number of young females present in
the clan when immigrants first arrive there, and female
choice of mates (Engh et al. 2002; East et al. 2003;
Höner et al. 2007; Van Horn et al. 2008). Adult natal
male hyenas are socially dominant to immigrant males,
and most of them show strong sexual interest in clan
females (Holekamp & Smale 1998), yet they sire only
3% of cubs in their natal clans. By contrast, immigrants
sire 97% of cubs, indicating that females prefer to mate
with immigrants over adult natal males (Engh et al.
2002; Van Horn et al. 2008). Among resident immigrant
males, social rank is correlated with male reproductive
success, but regression analysis showed that tenure in
the clan predicts this far better than does male rank
(Engh et al. 2002). Immigrants do not typically begin to
sire offspring until they have resided in their new clan
for 1 or 2 years, during which time they occupy the
lowest rank positions in the male queue (Engh et al.
2002; East et al. 2003).
To quantify reproductive skew, paternity was
assigned to 71 cubs as in Engh et al. (2002). These cubs
were conceived from 14 July 1987 to 7 June 2000; they
were the offspring of 29 females and 20 males. All but
one cub was the offspring of an immigrant male. An
additional 33 adult natal males and 26 immigrant males
did not sire any cubs. Although the reproductive benefit per female hyena ranged from 1 to 7 cubs, the skew
observed among the 29 females was not significantly
different from that expected at random (B = )0.0067,
P = 0.991) or through equal accrual of benefits (i.e. the
lower 95% CI = )0.0131 < 0), and it is clear that the
production of cubs was not monopolized (i.e. the upper
95% CI = 0.0006 < 0.976). Presumably the degree of
skew observed among Talek females is due largely to
variation in lifespan among the adult females (also see
Swanson et al. 2011). The range in number of offspring
was greater among males than females (1–15 cubs per
male), and the reproductive skew among the 79 males
was statistically greater than that expected through random accrual of benefits (B = 0.0544, P = 0.0001), or
equal accrual of benefits (i.e. the lower 95%
CI = 0.0323 > )0.0136), but reproduction was not
monopolized by any single male (i.e. the upper 95%
CI = 0.0843 < 0.9835). Reproductive skew among male
spotted hyenas was thus lower than among males of
12 K . E . H O L E K A M P E T A L .
Table 2 Reproductive skew (B) among polygnous male mammals
Species
B1
B range2
Sample size
Reference
Mountain gorilla, Gorilla beringei
White-faced capuchin, Cebus capucinus
European badger, Meles meles
Rhesus macaque, Macaca mulatta
Spotted hyena, Crocuta crocuta
Greater horseshoe bat, Rhinolophus
ferrumequinum
Collared peccary, Pecari tajacu
0.38
0.24
0.18
0.08
0.05
0.02
0.34–0.43
0.13–0.40
)0.062–0.63
0.08–0.08
n⁄a
n⁄a
4 groups, 22 males
8 groups, 58 males
25 groups
2 groups
1 group, 79 males
1 group
(Bradley et al. 2005)
(Muniz et al. 2010)
(Dugdale et al. 2008)
(Dubuc et al. 2011, Widdig et al. 2004)
Current study
(Rossiter et al. 2006)
0.01
)0.10–0.33
6 groups, 25 males
(Cooper et al. 2011)
1
2
Mean B values are reported where data from multiple social groups were available.
Minimum and maximum values of B reported where data from multiple social groups were available.
most other polygynous species for which B has been
quantified (Table 2), perhaps because role reversed sexual dimorphisms in body size and dominance status are
so rare in other mammals (Holekamp & Engh 2009).
Interestingly, as in spotted hyenas, collared peccaries are
sexually monomorphic, and in greater horseshoe bats,
females are larger than males, and in both these species,
B values are quite low, as they are in spotted hyenas.
Female choice of mates appears to be the key determinant of patterns of paternity in this species. At least
40% of female spotted hyenas mate with multiple males
during any given oestrous period, and 25–40% of twin
litters are multiply sired (Engh et al. 2002; East et al.
2003). Males of all ranks sire offspring, but surprisingly,
the alpha male in each immigrant cohort generally sires
fewer cubs than do males in lower rank positions (Engh
et al. 2002). Immigrant male rank is not correlated with
age, and immigrants as old as 18 years have high-quality sperm and ejaculates (Curren LJ, Weldele ML, Holekamp KE 2011, unpublished electroejaculation data.), so
their fertility does not appear to decline as they age.
Thus the fact that alpha males sire relatively few cubs
suggests an important role for female choice in determining reproductive success among males. Not only do
females clearly prefer immigrant males over adult natal
males, but they also frequently choose lower-ranking
immigrants over the alpha male in the immigrant queue
(Engh et al. 2002; Van Horn et al. 2008). High-ranking
male hyenas cannot monopolize reproduction if females
prefer not to mate with them. Absolute female control
over mating has thus reduced selection for male fighting ability, and has led to low levels of combat among
resident immigrant males, and to the evolution of a
male social queue (East & Hofer 2001; East et al. 2003).
Given the powerful influence of female mate choice
in spotted hyenas, it appears that males have been
obliged to develop strategies to maximize their reproductive success that supplement or replace male–male
combat. We find much heavier reliance in this species
than in most other mammals on alternative modes of
sexually selected interactions, such as endurance rivalry
(e.g. queuing, East & Hofer 2001), and sperm competition may also play an important role in spotted hyenas
(Curren LJ, Weldele ML, Holekamp KE 2011, unpublished electroejaculation data.). Female dominance and
male-like genitalia make sexual coercion impossible in
this species (East et al. 1993; Frank 1997). Instead, each
female determines whether or not a single male will
monopolize her during a given estrous period, and if
so, which male this will be. Females can tolerate or
refuse male mating attempts according to their own
reproductive interests, and this unusual degree of
female control appears to reduce the strength of the
relationship between social status and reproductive success among males.
Preliminary data from our long-term study indicate
that female spotted hyenas tend to produce paternally
unrelated offspring. For example, despite persistent
availability of individual males during successive reproductive cycles, females seldom permit a single male to
sire more than one of their litters. In all known cases
where sires were still present in the clan when a female
conceived her next litter after successfully weaning at
least one member of her last litter, only 3 of 30 females,
bearing 4 of 49 litters and having one to four chances to
remate, ever chose to mate again with a sire of one of
their earlier litters. One result of this apparent tendency
to have new males sire each successive litter is that
large clans are characterized by networks of kin comprised mostly of mothers, offspring and maternal halfsiblings sired by different males. In the final section of
this paper, we assess the dynamics and stability of kin
associations within the clan’s overall social network,
and inquire how these vary with resource availability.
Effects of kinship and prey abundance on social
network structure
Social scientists have long-recognized the importance
of social network theory in explaining human social
2011 Blackwell Publishing Ltd
H Y E N A S O C I E T Y , D E M O G R A P H Y A N D G E N E T I C S 13
2011 Blackwell Publishing Ltd
intense in this species and promotes the tendency for
hyenas to spend time away from group-mates (Kruuk
1972; Tilson & Hamilton 1984; Frank 1986; Smith et al.
2008), we also expected that social relationships among
hyenas would respond dynamically to changes in
resource abundance. That is, hyenas should maintain
the strongest ties with clan members when feeding
competition is relaxed during periods of abundant prey,
as indicated by our biweekly prey censuses.
Overall, our social network analysis revealed that the
Talek clan is a dynamic social group comprised of kinbased subgroups, which in turn are comprised of individuals in multiple life-history stages. The strength of
each hyena’s ties within its social network decreased
significantly as it progressed through each successive
life history stage; this was particularly striking among
natal males (Kruskal–Wallis test: H2,395 = 161.2, P <
0.0001, Fig. 8). On average, den-dependent cubs
(N = 136) had significantly stronger ties to clan-mates
than did den-independent subadults (N = 151) or natal
adults (Fig. 8; N = 108, Mann–Whitney U-tests: Z =
)9.27 and )11.1, respectively, P < 0.00001 for both).
Moreover, subadults were more strongly connected to
clan-mates than were adult hyenas (Z = )9.27, P <
0.00001). We detected no sex difference in strength of
0.26
0.24
Standardized strength of social
relationships
organizations (reviewed by Newman 2003b), but formal
social network theory has only recently been applied to
explain the structuring of animal societies (Krause et al.
2007; Croft et al. 2008; Wey et al. 2008; Sih et al. 2009).
Although human social networks are often characterized by homophily, with individuals preferentially associating with others that possess traits similar to their
own (e.g. McPherson et al. 2001; Newman 2003a), we
do not yet know if this is true among kin-biased network structures of wild animals (but see Smith et al.
2010; Wey & Blumstein 2010; Wiszniewski et al. 2010;
Wolf & Trillmich 2008). Within spotted hyena clans,
dyadic patterns of association reflect social preferences
(e.g. Holekamp et al. 1997a; Szykman et al. 2001; Smith
et al. 2007). For example, patterns of association predict
the extent to which hyenas engage in affiliative behaviours such as greeting and coalition formation (Smith
et al. 2010, 2011). Hyenas are also most tolerant of close
associates, withholding aggression from these groupmates both at and away from food (Smith et al. 2007).
However, it remains unclear to what extent dyadic preferences generate subgroup cliques or communities,
which in turn might structure the social group as a
whole. Understanding such processes is important for
identifying the levels of selection acting to maintain
sociality in general, and cooperation in particular,
among group-living animals (Croft et al. 2004; West &
Gardner 2007). Moreover, many workers assume that
relationships among individual members of vertebrate
social groups reflect long-term strategic interests of
individual group members (e.g. Silk et al. 2006a,b,
2010). Although such relationships should theoretically
be resilient in the face of short-term fluctuations in ecological conditions, recent evidence has called this notion
into question (Henzi et al. 2009). Instead, it is possible
that individuals only base social preferences on the
immediate value of the commodities offered by potential trading partners (e.g. Noë & Hammerstein 1994;
Barrett et al. 1999). Furthermore, such effects have
never been explored in mammalian carnivores. Here we
applied social network theory to assess the dynamics
and stability of kin associations among natal animals
within our Talek study clan.
We inquired specifically about the extent to which
members of distinct matrilines within hyena clans represent differentiated cliques or subgroups comprised of
individuals who are more closely connected to one
another than to members of other subgroups within the
clan. Because maternal kin occupy similar social ranks
(Fig. 1) and function as important social allies to one
another (Engh et al. 2002; Wahaj & Holekamp 2006;
Smith et al. 2010), we predicted that maternal kin
would generally form stronger ties than non-kin within
their social networks. Because feeding competition is
0.22
Kin_High prey
A A
Kin_Low prey
0.20
Non-kin_High prey
0.18
Non-kin_Low prey
0.16
0.14
C
0.12
0.10
0.08
D
B
G
H
B
E
0.06
F
I
K
J
0.04
L
M
N
0.02
0.00
Den cubs
Subadults
Adult females
Adult males
Life history stage
Fig. 8 Mean ± SE standardized strength of social relationships, a measure of the tendency for individual natal hyenas to
associate with other natal hyenas. Relationships depicted are
limited to those among natal animals that were concurrently
alive with maternal kin (based on matriline membership) and
non-kin during periods of low (February–May, October–January) and high (June–September) prey abundance as a function
of each focal hyena’s life history stage. Standardized strength
among den cubs (N = 136) and subadults (N = 151) were statistically similar between the sexes, but adult females (N = 62)
maintained stronger social ties than did adult natal males
(N = 46) within their social networks. Immigrant males were
excluded from this analysis. Letters above bars indicate statistically significant differences for matched comparisons (see text)
after correcting for multiple testing at P < 0.05.
14 K . E . H O L E K A M P E T A L .
(A)
connections involving den-dwelling cubs (NM = 70,
NF = 66) or subadults (NM = 76, NF = 75) within their
social networks (Z = 0.77 and 1.88, P = 0.44 and 0.12,
respectively), but adult females (N = 62) were significantly more strongly connected within the clan than
were adult natal males (N = 46, Z = 4.34, P = 0.00001).
Therefore, we pooled data from males and females for
subsequent analysis involving cubs and subadults, but
performed separate analyses for adults of each sex. In
general, individuals in all three life history stages preferentially maintained social connections with maternal
kin over non-kin (Fig. 8). That is, cubs, subadults, and
adults were more strongly connected to maternal kin
than to non-kin, as indicated by significantly greater
standardized strength within, than between, matrilines
(Z ‡ 0.49, and P £ 0.000001 for all cases).
In addition to kinship, prey abundance also influences inter-individual relationships among natal hyenas, as illustrated by the networks within a single
‘‘cohort’’ of natal animals from a year-long period
(Fig. 9). This cross-sectional analysis extends the longitudinal data in Fig. 5, by showing that even after
excluding den cubs, members of the alpha matriline still
have far more kin available as social allies than do natal
animals from low-ranking matrilines (Fig. 9). Importantly, despite the fission-fusion nature of their society,
individual hyenas maintain stable group membership
by fostering both direct ties to preferred companions
(Fig. 8) and indirect ties to clan-mates with whom they
rarely come into direct contact (Fig. 9).
Among both subadults and adults, but not among
den-dwelling cubs, network dynamics varied predictably in response to variation in local prey abundance
(Fig. 9). Both maternal kin (Z = 0.16) and non-kin
(Z = 0.88) maintained strong ties with den-dwelling
cubs irrespective of prey abundance (Wilcoxon SignRanks Test: P ‡ 0.379 for both, Fig. 8). However, both
subadults and adults were more strongly socially connected to maternal kin during periods of relative prey
abundance than during periods of prey scarcity (Wilcoxon Sign-Ranks Test: Z ‡ 2.58 and P £ 0.01 for all comparisons), and their connections to non-kin were also
stronger during periods of high than low prey (Z ‡ 3.13
and P £ 0.001 for all). Thus subadults and adults were
more strongly connected to clan-mates during times
when competition for food was least intense; however,
regardless of prey availability, they remained more
strongly connected to their relatives than to non-kin.
Our finding that hyenas maintain differentiated relationships with preferred social companions throughout
the year differs from that of Henzi et al. (2009), whose
social network analysis of two cohorts of female chacma
baboons (Papio hamadryas ursinus) suggested that companionships identified during times of food scarcity
(B)
(C)
Fig. 9 Variation in social networks within the Talek clan during periods of low (A and C) and high (B) prey abundance.
Each matriline present in the clan during this 12-month period
is assigned a unique number. The highest possible matriline
rank is 1. Large nodes represent adults and small nodes represent subadults. Line darkness is directly proportional to the
strength of the association index (tie) between each connected
pair of hyenas. Den-dwelling cubs were not included in these
networks because their relationships did not significantly vary
between periods of low and high prey abundance (Fig. 8).
2011 Blackwell Publishing Ltd
H Y E N A S O C I E T Y , D E M O G R A P H Y A N D G E N E T I C S 15
were replaced by casual acquaintanceships when food
was plentiful, and that the strength of social relationships declined as food abundance increased. In contrast,
our data demonstrate that hyenas were most strongly
connected to social partners during periods when food
was most abundant, indicating that social relationships
among hyenas are constrained by feeding competition.
Interestingly, in this respect, hyena networks more closely resembles those of honeybees (Apis mellifera) and
European shore crabs (Carcinus maenas) than those of
Chacma baboons. Among honeybees, network density
increased with food abundance (Naug 2008). Similarly,
in the otherwise non-social shore crab, partner number
(node degree) and clique size increased when dispersed
food was experimentally clumped (Tanner & Jackson
2011). Among spotted hyenas, the positive relationship
between network density and prey abundance might be
mediated either by improved payoffs from information
exchange when food is abundant or by the stronger
need to forage solitarily when prey are relatively scarce.
Conclusions and unanswered questions
Spotted hyenas live in large, complex societies structured like those of cercopithecine primates. As in the
societies of many mammals, the social ranks of individual females have profoundly important fitness consequences, and rank in fact affects the persistence of entire
matrilineal kin groups within hyena clans. Among other
mammalian carnivores, in which group size is smaller
than in our study groups, average R values may vary
greatly within social groups, but average relatedness
within groups is much higher than in spotted hyenas
(e.g. Spong et al. 2002; Griffin et al. 2003; Baker et al.
2004; Dugdale et al. 2008). The greater variation in size
of spotted hyena clans generates an exponentially
greater variation in the number of dyads present per
clan, and in the dyadic relatedness among individuals.
Large clans are dynamic networks of relationships
among individuals who may be very closely, or only
very distantly, related to one another. Nepotism is common in hyena societies, and relationships among matrilineal kin are more affiliative, cooperative and stable
than are relationships among individuals that are maternally unrelated (East et al. 1993; Holekamp & Smale
1993; Smale et al. 1993; Engh et al. 2000; Van Horn et al.
2004b; Wahaj et al. 2004; Smith et al. 2010). Consistent
with this, we found here that maternal kinship is a critical determinant of network structure within hyena
clans, and that the importance of maternal kin affiliations was clear even when social relationships were
most severely constrained by ecological conditions.
In large hyena clans, mean relatedness among
individual members is very low due to ubiquitous male
2011 Blackwell Publishing Ltd
dispersal and strong female preferences for immigrants
as mates, as well as for males with which they have not
mated previously. Although there are undoubtedly limits to the abilities of male hyenas to move across
human-dominated landscapes, male-biased dispersal,
low reproductive skew and great behavioural plasticity
should help maintain viability of spotted hyena populations even within African national parks that have effectively become islands isolated from one another by
dense human settlements and inhospitable agricultural
landscapes. Although this needs to be determined
empirically, if this hypothesis is correct, then despite
their status as top predators, spotted hyenas might be
expected to fare better in their struggle against extinction than other large carnivores with more restricted
dispersal abilities, greater reproductive skew or less
behavioural plasticity. Although the effects of increasing
anthropogenic activity on demography, social relationships and genetic structure within clans and populations may be considerable, we have only recently begun
to explore them (e.g. Pangle & Holekamp 2010; Holekamp & Dloniak 2010).
Many questions remain unanswered about society,
demography and genetic structure in the spotted hyena.
Our data suggest an important effect of chance in determining which subordinate matrilines persist over many
generations. Although chance has been shown to play
an important role in shaping the evolution of experimental laboratory populations (e.g. Travisano et al.
1995), we know very little about how chance affects fitness in free-living mammals. In addition to social rank,
body size has recently been shown to influence fitness
among female spotted hyenas (Swanson et al. 2011).
However, it is not yet known whether size affects fitness in both sexes, nor how effects of larger body size
are mediated to affect fitness in females. Finally, as is
true in most mammals due to male-biased dispersal,
lifetime data on reproductive success are much more
difficult to obtain from male spotted hyenas than from
females, so we know little about the contributions made
by sons to their mothers’ fitness. Although strong rankrelated maternal effects are known to influence reproductive success among female spotted hyenas (e.g.
Fig. 5), we know much less about maternal rank effects
on males over the course of their lifetimes. Höner et al.
(2010) recently presented data indicating that sons of
high-ranking females enjoy greater reproductive success
during their early years in their new clans than do their
lower-ranking counterparts. However, the mechanisms
mediating maternal rank effects on reproductive success
among male hyenas are completely unknown.
Little is currently known about the mechanisms
mediating variation in relatedness among clans
within populations. We cannot assume that observed
16 K . E . H O L E K A M P E T A L .
movements of male hyenas translate directly into gene
flow because several different variables might make
observations unreliable indicators of genetic structure.
Although a male may move from one clan to another, it
is unclear whether he will achieve reproductive success
in the new clan. Similarly, immigrants from distant
clans may have different reproductive success than
immigrants from neighbouring clans. Indeed, without
looking at the genetic data it is impossible to know how
male dispersal and reproductive success affect relatedness across clans. Roughly 40% of immigrant males are
known to engage in secondary dispersal (Van Horn
et al. 2003), but the effects of this behaviour on gene
flow are unknown, as are the forces prompting established resident immigrants to move to yet another new
clan. Although secondary dispersal might be expected
among males with which females refuse to copulate,
the basis on which females choose their mates also
remains poorly understood in this species.
In spite of the low overall levels of relatedness among
clan-mates, maternal kinship generates sub-groups of
allies who cooperate to win in resource competition
within clans. Even ubiquitous male dispersal and paternal gene flow can neither overwhelm the influence of
female philopatry nor eliminate the potential indirect
fitness benefits of cooperating with kin over unrelated
clan-mates (Van Horn et al. 2004a). We do not currently
know whether individuals with large networks of kin
allies enjoy comparatively large fitness benefits over
extended time periods, after controlling for effects of
social rank. Nor do we know whether matrilineal kin
groups with the strongest social relationships under
each particular set of ecological conditions do better on
average in the long-term than those whose members
associate less closely. However, our data certainly suggest these as possibilities. Extinctions of entire matrilines during a period spanning less than 10 generations
(Fig. 5) further suggest that strong selection may be
operating on both individuals and kin groups within
large clans. If so, then after controlling for family size
and social rank, the most cohesive or most cooperative
families might be expected to enjoy the greatest fitness,
even when losses accrue to some individual family
members as a result of their greater social cohesion, for
example, due to resource losses or injuries during competition within matrilines over food. Furthermore, we
might expect to be able to use network analysis to
detect trade-offs between individual and family level
adaptations in this and other gregarious species. It
would be fascinating to determine, for example,
whether matrilines such as the one descended from
female F40 in Fig. 5 persist over multiple generations
while others die out because social bonds among their
members are unusually weak or strong, given its rank
within the clan. In any case, there can be no doubt that
the most significant and predictable subgroups within
spotted hyena clans are matrilineal kin groups.
Acknowledgements
We thank the Kenyan Ministry for Education, Science and
Technology, the Kenya Wildlife Service, the Narok County
Council, the senior warden of the Masai Mara National
Reserve, Brian Heath and the Mara Conservancy for permission to conduct this research. We thank the many individuals
who have contributed to collection of field data since 1988,
with special thanks to Laura Smale for her contributions to
data analysis and interpretation as well as to the fieldwork. We
thank Stephen Thomas for his substantial help designing
Fig. 5. Financial support for this work was provided by the
University of California Los Angeles Center for Society and
Genetics, the David and Lucille Packard Foundation, the Kenya
Wildlife Trust and NSF Grants BNS8706939, BNS902146,
IBN9309805, IBN9630667, IBN9906445, IBN0113170, IBN034338,
IOB0618022, IOS0819437, IOS1121474 and OIA0939454.
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K.E.H. works on the physiological mediation, ontogenetic
development, and functional significance of animal behavior.
J.E.S. studies the evolutionary origins, maintenance, and stability of social behavior in mammals. C.C.S. uses mathematical
models, statistical inference and computation to investigate
problems in microbial evolution, infectious disease dynamics,
and behavior. R.C.V.H explores the relationships in animals
among kinship, individual experience, and dispersal, emphasizing the implications for evolution and conservation. H.E.W.
investigates the relationships between environmental variation,
life history patterns, and the behavior of individuals.
Data accessibility
All data supporting the results in the paper are archived with
Dryad as doi:10.5061/dryad.tg582.
2011 Blackwell Publishing Ltd